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Table 2 Prevalence of diabetic retinopathy (DR) and sight-threatening diabetic retinopathy (STDR) in eight hospitals
DR STDR
Age–gender- Number of Age–gender-
Number of subjects Number of subjects Crude prevalence standardised subjects with Crude prevalence standardised
Region with DM with DR (%) prevalence (%) STDR (%) prevalence (%)
Southern region 6531 1755 26.87 26.90 766 11.73 11.74
Luzhou 2962 863 29.13 29.09 344 11.61 11.60
Zhanjiang 1435 374 26.06 26.08 214 14.91 14.94
Guilin 2134 518 24.27 25.19 208 9.74 9.73
Northern region 8547 2449 28.65 28.84 1132 13.24 13.31
Jilin 3489 804 23.04 23.05 295 8.46 8.45
Jinan 2143 563 26.27 27.00 211 9.85 10.18
Luoyang 1042 332 31.86 31.90 191 18.33 18.37
Huhehaote 716 203 28.35 28.68 103 14.38 14.46
Zhengzhou 1157 547 47.28 47.17 332 28.69 28.56
Total 15 078 4204 27.88 27.90 1897 12.58 12.63
from 23.1% to 47.2%, and that of STDR from 8.5% to 28.6%. However, the prevalence of any DR and STDR among eight
There was a significant difference in age-standardised prevalence of hospitals showed significant differences. Risk factors for DR and
any DR (χ2=204.34, p<0.001) and STDR (χ2=298.69, p<0.001) STDR previously identified in other studies—longer diabetes
between the eight hospitals (table 2). duration, higher HbA1c and higher systolic blood pressure—
Binary multiple logistic regression indicated that younger age were also identified in our study.4 5 11–13
(OR, 0.967; 95% CI 0.961 to 0.973), longer duration of DM The prevalence of DR in our study was similar to that in other
(OR, 1.093; 95% CI 1.084 to 1.103), higher HbA1c (OR, 1.115; studies from Western countries (the Blue Mountains Eye Study
95% CI 1.078 to 1.154), higher FPG (OR, 1.074; 95% CI 1.048 in Australia and the Multi-ethnic Study of Atherosclerosis in the
to 1.101), higher systolic blood pressure (OR, 1.014; 95% CI USA)14 15 and other Asian countries (the Singapore Indian Eye
1.009 to 1.018), faster heart rate (OR, 1.010; 95% CI 1.004 to Study and the Singapore Malay Eye Study).12 16 However, the
1.016), higher LDL (OR, 1.149; 95% CI 1.079 to 1.224), lower prevalence of DR in China reported by studies published in the
triglycerides (OR, 0.926; 95% CI 0.874 to 0.982), higher BUN last 10 years showed large discrepancies, which ranged from
(OR, 1.012; 95% CI 1.001 to 1.023) and elevated serum creatinine 11.9% to 43.1%. Hu et al reported that the prevalence of DR
level (OR, 1.003; 95% CI 1.002 to 1.005) were associated with the was only 11.9% in a population-based cross-sectional study in
presence of DR (table 3). Similar risk factors, except for WHR and Liaoning Province, China.11 However in another investigation
triglycerides, were associated with STDR (table 4). in rural China, the population-based Handan Eye Study found a
prevalence of DR of 43.1%. That figure was much higher than
Discussion data reported in other studies from China, including our investi-
The overall age–gender-standardised prevalence of any DR gation.17 The discrepancy may be due to different study designs,
and STDR was 27.9% and 12.6%, respectively in our study. grading standards and populations sampled. Our findings also
highlighted that the prevalence in the Northern region (28.7%) study, suggesting acceptable validity of our results. Additionally,
was higher than that in the Southern region (26.9%). Similar younger age, faster heart rate, higher LDL, lower triglycerides,
results were reported by Liu et al in a meta-analysis of DR higher BUN and higher serum creatinine were associated with
prevalence in mainland China.18 The risk factors were similar DR in this study. The association of serum lipids with DR was
between the Southern region and the Northern region by respec- obtained in this study, although the Multi-Ethnic Study of
tively binary multiple logistic regression analysis. However, the Atherosclerosis and the Singapore Indian Eye Study showed no
mean duration of DM (8.91 years) in the Northern region is associations of serum lipids with DR.12 20 These inconsistent
significantly longer than that (7.15 years) in the Southern region findings imply that serum lipids are not strongly associated with
(t=15.956, p<0.05). The discrepancy of the prevalence of DR DR. Similar to the Singapore Indian Eye Study and the Beijing
between the Northern and Southern regions may mainly be Eye Study, DR was associated with younger age in our investi-
caused by the difference in the duration of DM. gation.5 17 This association requires further exploration. In our
The overall prevalence of STDR was relatively high at 12.6% study, we found that both BMI and WHR were not associated
in our study. The high prevalence of STDR was mainly driven with DR. This association had been found in other DR inves-
by the high prevalence of maculopathy. According to the UK tigations.11 21 Although several previous studies including one
guidelines, maculopathy is defined as having one or more of study from China reported an association of BMI with DR pres-
the following: exudates within one disc diameter (DD) of the ence,5 16 22 23 we did not find this association in our study. Our
centre of the fovea, circinate or groups of exudates within the finding implies that both WHR and BMI may not be good at
macula, or any microaneurysms or haemorrhages within one DD predicting DR risk in China. We also observed that the pres-
of the centre of fovea if visual acuity ≤6/12.8 However, other ence of DR was associated with serum creatinine and heart rate.
studies such as the Beijing Eye Study and Singapore Eye Study Moreover, this association was also found for STDR in our study.
had different definitions of maculopathy, for example, using the An association between serum creatinine and DR was reported
ETDRS guidelines. Moreover, only clinically significant macular previously by a national DR screening investigation from South
oedema rather than macular oedema is included in STDR in Korea.24 The finding implied that renal function may play a
these studies. It is therefore difficult to assert that the prevalence certain role in DR progression. Two previous studies reported
of STDR in our study was higher than that in other studies in an association between DR and heart rate.25 26 However, the
mainland China, due to different grading systems. Comparing causes of faster heart rate can be physiological and pathological.
our results to the screening in Hong Kong which also followed In our screening, heart rate of each participant was not recorded
the UK guidelines, the prevalence of maculopathy (11.2%) in in the same standard conditions. Thus, the association between
our study is higher than the findings (8.6%) in Hong Kong. Rela- heart rate and DR needs further exploration to confirm. Similar
tively poor awareness and bad control of DM of participants in risk factors, except for BUN and triglycerides, were found for
the mainland might be the reason. According to Xu et al’s report, STDR in this study. The inconsistency in risk factors for DR and
7 out of 10 patients with diabetes are not aware of their high STDR implies that there are some other mechanisms for DR
blood glucose, only 25.8% receive treatment for diabetes and progressing to STDR.
only 39.7% of those treated have adequate glycaemic control in The strengths of our study include the very large sample size
mainland China.19 compared with previous studies in China, the high proportion of
In multivariate analysis, established risk factors for DR such gradable fundus pictures, the use of standardised grading proto-
as longer duration of diabetes, higher HbA1c level, hypergly- cols and the detailed assessment of risk factors. The limitations of
caemia and higher systolic blood pressure were confirmed in our our study should be mentioned. First, the cross-sectional design
1594 Zhang G, et al. Br J Ophthalmol 2017;101:1591–1595. doi:10.1136/bjophthalmol-2017-310316
Global issues
prevented direct conclusions on risk factors. Second, our macu- 4 Wang FH, Liang YB, Peng XY, et al. Risk factors for diabetic retinopathy in a rural
lopathy criteria may have overestimated the true prevalence of Chinese population with type 2 diabetes: the Handan Eye Study. Acta Ophthalmol
2011;89:e336–43.
DM. The prevalence of DM cannot be directly compared there- 5 Xu J, Wei WB, Yuan MX, et al. Prevalence and risk factors for diabetic retinopathy: the
fore with that in other studies. Third, as a hospital-based study, Beijing Communities Diabetes Study 6. Retina 2012;32:322–9.
the patients recruited into our study may not be representative of 6 Stefánsson E, Bek T, Porta M, et al. Screening and prevention of diabetic blindness.
the overall population with diabetes. Finally, we did not include Acta Ophthalmol Scand 2000;78:374–85.
as variables other possible risk factors, such as family income, 7 American Diabetes A: diagnosis and classification of diabetes mellitus. Diabetes care
2014;37(Suppl 1):S81–90.
education and psychosocial factors. 8 Harding S, Greenwood R, Aldington S, et al. Grading and disease management
In summary, our investigations have shown that approximately in national screening for diabetic retinopathy in England and Wales. Diabet Med
one-third of patients with DM in our large Chinese sample had 2003;20:965–71.
DR, and more than 10% had STDR. Similar risk factors for DR 9 Lian JX, Gangwani RA, McGhee SM, et al. Systematic screening for diabetic
and STDR in Western populations with diabetes were found in retinopathy (DR) in Hong Kong: prevalence of DR and visual impairment among
diabetic population. Br J Ophthalmol 2016;100:151–5.
Chinese patients with diabetes. 10 Committee UNS. Essential elements in developing a diabetic retinopathy screening
programme. Workbook version 4.4. UK: UK National Screening Committee. 2012
Acknowledgements The authors would like to thank Dr Michael Williams (Centre http://diabeticeyescreeningnhsuk/qualityassurance
for Medical Education, Queen’s University of Belfast, UK) and Professor Chi-Pui Pang 11 Hu Y, Teng W, Liu L, et al. Prevalence and risk factors of diabetes and diabetic
(Department of Ophthalmology and Visual Sciences, The Chinese University of Hong retinopathy in Liaoning province, China: a population-based cross-sectional study.
Kong) for the critical comments and language polishing of the manuscript PLoS One 2015;10:e0121477.
Contributors GZ contributed to the design of the work, acquisition of data and 12 Zheng Y, Lamoureux EL, Lavanya R, et al. Prevalence and risk factors of diabetic
analysis and interpretation of data; drafting the work and revising it critically for retinopathy in migrant Indians in an urbanized society in Asia: the Singapore Indian
important intellectual content. HC contributed to the analysis and interpretation eye study. Ophthalmology 2012;119:2119–24.
of data. WC critically revised the manuscript for important intellectual content. MZ 13 Ting DS, Cheung GC, Wong TY. Diabetic retinopathy: global prevalence, major
made substantial contribution to the conception and design of the work; analysis risk factors, screening practices and public health challenges: a review. Clin Exp
and interpretation of data; drafting the work and revising it critically for important Ophthalmol 2016;44:260–77.
intellectual content. 14 Wong TY, Klein R, Islam FM, et al. Diabetic retinopathy in a multi-ethnic cohort in the
United States. Am J Ophthalmol 2006;141:446–55.
Funding The programme was supported by Chinese Foundation for Lifeline Express 15 Mitchell P, Smith W, Wang JJ, et al. Prevalence of diabetic retinopathy in an older
and Lifeline Express Hong Kong Foundation. community. The Blue Mountains Eye Study. Ophthalmology
Competing interests None declared. 1998;105:406–11.
16 Wong TY, Cheung N, Tay WT, et al. Prevalence and risk factors for diabetic retinopathy:
Patient consent Obtained.
the Singapore Malay Eye Study. Ophthalmology 2008;115:1869–75.
Ethics approval Hospital ethics committees. 17 Wang FH, Liang YB, Zhang F, et al. Prevalence of diabetic retinopathy in rural China:
Provenance and peer review Not commissioned; externally peer reviewed. the Handan Eye Study. Ophthalmology 2009;116:461–7.
18 Liu L, Wu X, Liu L, et al. Prevalence of diabetic retinopathy in mainland China: a meta-
Data sharing statement The unpublished data are still being acquired for analysis. PLoS One 2012;7:e45264.
continuous screening programme. The data ownership belongs to the Chinese 19 Xu Y, Wang L, He J, et al. Prevalence and control of diabetes in Chinese adults. JAMA
Foundation for Lifeline Express and Lifeline Express Hong Kong Foundation. The 2013;310:948–59.
authors are authorised to use the data from the programme. 20 Sasongko MB, Wong TY, Nguyen TT, et al. Serum apolipoprotein AI and B are
Open Access This is an Open Access article distributed in accordance with the stronger biomarkers of diabetic retinopathy than traditional lipids. Diabetes Care
Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which 2011;34:474–9.
permits others to distribute, remix, adapt, build upon this work non-commercially, 21 Man RE, Sabanayagam C, Chiang PP, et al. Differential association of generalized and
and license their derivative works on different terms, provided the original work abdominal obesity with diabetic retinopathy in Asian patients with type 2 diabetes.
is properly cited and the use is non-commercial. See: http://creativecommons.org/ JAMA Ophthalmol 2016;134:251–7.
licenses/by-nc/4.0/ 22 Cheung N, Wong TY. Obesity and eye diseases. Surv Ophthalmol
2007;52:180–95.
© Article author(s) (or their employer(s) unless otherwise stated in the text of the
23 Lim LS, Tai ES, Mitchell P, et al. C-reactive protein, body mass index, and diabetic
article) 2017. All rights reserved. No commercial use is permitted unless otherwise
retinopathy. Invest Ophthalmol Vis Sci 2010;51:4458–63.
expressly granted.
24 Jee D, Lee WK, Kang S. Prevalence and risk factors for diabetic retinopathy: the Korea
National Health and Nutrition Examination Survey 2008-2011. Invest Ophthalmol Vis
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